PHOSPHORUS UPTAKE FROM STRUVITE IS MODULATED BY THE NITROGEN FORM APPLIED - JUSER
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80 DOI: 10.1002/jpln.201900109 J. Plant Nutr. Soil Sci. 2020, 183, 80–90
Phosphorus uptake from struvite is modulated by the nitrogen form
applied
Ana A. Robles-Aguilar1,2, Silvia D. Schrey1, Johannes A. Postma1, Vicky M. Temperton3, and Nicolai D. Jablo-
nowski1*
1 Forschungszentrum Jülich GmbH, Institute of Bio- and Geosciences, IBG-2: Plant Sciences, 52425 Jülich, Germany
2 Current affiliation: Laboratory of Analytical Chemistry and Applied Ecochemistry, Faculty of Bioscience Engineering, Ghent University,
Coupure Links 653, 9000 Ghent, Belgium
3 Institute of Ecology, Faculty of Sustainability, Leuphana University Lüneburg, Universitätsallee 1, 21335 Lüneburg, Germany
Abstract
Next to nitrogen, phosphorus (P) is the most limiting nutrient for plant production worldwide. To
secure food production, new nutrient management strategies using alternative P sources instead
of mined P fertilizers need to be implemented. Struvite (MgNH4PO4 × 6 H2O) is a promising
example of a recycled mineral P fertilizer. Besides positive agronomic results regarding crop
yields, further investigations are required to improve the use efficiency of the product and thereby
increase its value. Using an automated plant phenotyping platform, we investigated the dynamic
response to struvite by two plant species (lupine and maize) with diverse P acquisition strategies
in an acidic sandy substrate. Although at three weeks after germination both maize and lupine
had reduced leaf area in the struvite treatments compared to the commercial triple superphos-
phate (TSP), from week four onwards struvite plants grew larger than the TSP-treated plants,
indicating a slow release fertilizing effect. Greater P uptake efficiency (g / root length), but
reduced root length were observed in the combined treatment of struvite and ammonium, in com-
parison to struvite and nitrate. We propose that rhizosphere acidification in response to ammo-
nium uptake may enhance P recovery from struvite. A possible additional acidification effect by
lupine root exudation might explain the higher P uptake efficiency in this species compared to
maize. We conclude that struvite combined with ammonium can be used as a sustainable slow- Supporting Information
release P fertilizer on acidic sandy soils. available online
Key words: ammonium / nitrate / recycled phosphorus / root morphology modification / slow-release
fertilizer / struvite
Accepted November 11, 2019
1 Introduction
Phosphorus (P) is an essential macro-element that plays a research has been conducted on how to apply struvite most
key role in many essential plant processes (Misson et al., efficiently as a fertilizer and how well plants can metabolize it.
2005; Jouhet et al., 2007). Consequently, the growing
demand for food and feed production resulted in the need to Struvite solubility is low in water. Nevertheless, it is generally
apply P in the form of fertilizers (Vance et al., 2003). The main accepted that struvite is a good candidate to be used as a P
source of P comes from rock phosphate mines, a non-renew- source for plants. As reviewed by Kataki et al. (2016), struvite
able resource predicted to be depleted within a few hundred fertilization results in similar crop yields as mineral fertilization
years (Fixen and Johnston, 2012). on different plant species such as Lolium perenne (Johnston
and Richards, 2003), Zea mays (Antonini et al., 2012) or
To foster a more sustainable use of P, the European Union Triticum aestivum (Massey et al., 2009). Furthermore, struvite
has recently proposed to implement different strategies, has been proposed as a slow-release fertilizer, with a steady
including the recovery of P from waste (Bonvin et al., 2015; nutrient supply for plants (Li and Zhao, 2003; Antonini et al.,
Stutter et al., 2015; Withers et al., 2015). A promising example 2012). Most of these studies show comparable or even higher
is struvite (MgNH4PO4 × 6 H2O) that can be recovered from effectiveness of struvite than the water-soluble fertilizers at
wastewater (Batstone et al., 2015) or manure (Zarebska the end of the experiments (Möller et al., 2018).
et al., 2015). As reviewed by Zarebska et al. (2015), numer-
ous experiments have examined which technologies are the If we assume that struvite releases P slower than highly solu-
most efficient for struvite recovery regarding the source of ble fertilizers, low P solubility might be observed in the early
input. Within the larger question to which extent struvite can plant growth stage after using struvite as fertilizer. The low P
replace unsustainable rock phosphate-based fertilizers, less solubility can be overcome by some plant species with specif-
* Correspondence: Dr. N. D. Jablonowski; e-mail: n.d.jablonowski@
fz-juelich.de
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.com
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in
any medium, provided the original work is properly cited.J. Plant Nutr. Soil Sci. 2020, 183, 80–90 Effect of N source on P-availability from struvites 81
ic root traits to enhance P acquisition (Clarkson, 1981; Maize and lupine were investigated using an acidic, nutrient
Talboys et al., 2016). Species can differ strongly in their P poor sandy substrate (hereafter referred to as a ‘‘marginal
acquisition strategies, as reflected in their differences in vari- substrate’’), where struvite is more soluble than in alkaline or
ous root traits (Lynch, 1995; Abdolzadeh et al., 2009). Here neutral substrates. In experiment A we investigated: (1) stru-
we compare Zea mays (maize) and Lupinus angustifolius vite P fertilizing effect on plant biomass; (2) effect of N source
(narrow-leaf lupine), which differ in plant root physiology and applied on root architecture; (3) whether the nitrogen source
morphology. Narrow-leaf lupine has high physiological root applied modified the P uptake efficiency from struvite, de-
plasticity, related to exudation of large amounts of organic scribed as the P uptake per unit of root length, and whether it
acids (Pang et al., 2010a, 2010b). Besides that, roots of nitro- might be plant species dependent. In experiment B we
gen-fixing legumes like lupine further acidify the rhizosphere, investigated: (1) the continuous effect of struvite as a slow-
enhancing P mobilization in soil and additional subsequent P release fertilizer on plant biomass in lupine and maize; (2) if,
acquisition (Hinsinger, 2001). Contrary to lupine, maize is besides the known exudation capacity, lupine also relies on
known to exhibit extensive root morphological plasticity in additional changes in root architecture to increase P uptake
response to P fertilization, but does not seem to rely on car- efficiency from struvite in comparison with TSP, and whether
boxylate exudation for mobilizing insoluble P (Wen et al., it might be modified by applying nitrogen as NHþ 4 or NO3 .
2017). To allow us to investigate the struvite-P uptake on low
exudative and non-nitrogen fixing species, maize was used With this study we are aiming to first, identify those root traits
as a control. that are related to an increase in struvite-P uptake efficiency,
and second, analyze the fertilizing effects of struvite over
Studying possible effects of the applied P fertilizers on the time. We hypothesize that: (1) P uptake per unit root length
root morphology should help to identify those traits that are from lupine and maize will be similar; however, the morpho-
related to an increase in P uptake. As P concentrations can logical root changes in maize in response to ammonium will
act as growth regulators, the applied P sources (that might be greater than in lupine that might rely more on other strat-
have different phosphorus release rates into the rhizosphere) egies such as exudation of carboxylates; (2) we further hy-
can significantly alter root system architecture. For example, pothesize that lupine is a more suitable crop to use when ferti-
it was previously shown that root morphological responses of lized with struvite-P together with ammonium, comparable
maize (i.e., specific root length and proportion of fine roots) with the effect of the highly available TSP, that will not be af-
increased with decreasing shoot P concentration (Wen et al., fected by the N source jointly applied. Once we understand to
2017). Similarly, the nitrogen source applied can also act as a what extent species and growth conditions influence P recov-
growth regulator. Sattelmacher et al. (1993) reported ammo- ery from struvite used as a fertilizer, proper management ad-
nium concentration-dependent stimulatory effects on root vice for its application can be provided.
growth. In addition, the nutrient source applied can change
the rhizosphere pH (Gahoonia et al., 1992), which might also
influence root morphology as previously described for the 2 Material and methods
total root length of Lupinus angustifolius (Tang et al., 1992;
Robson and Tang, 1998). 2.1 Experimental set-up
Few studies have addressed these multiple interactions Experiment A followed a three-factorial (P-fertilizer, N-ferti-
between struvite and other fertilizers on plant growth (Talboys lizer, and plant species) completely randomized design with
et al., 2016). In the present study, we analyzed the effect of 10 repetitions. Fertilizer treatments comprised of struvite and
the N and P sources applied on root morphology and P an unfertilized control (No P), and each of them was combin-
uptake. Struvite decomposition is a proton consuming pro- ed with either ammonium or nitrate as the N form applied.
cess that increases the soil pH. Therefore, we tested if the The two different plant species in this study were lupine (Lupi-
assumed acidification in the rhizosphere induced by the appli- nus angustifolius L. subsp. angustifolius, cultivar: blau ‘‘Bore-
cation of ammonium could neutralize this pH increase and gine’’, Kiepenkerl, Germany) and maize (Zea mays, ‘‘Badisch-
facilitate the struvite solubility. We hypothesized that the appli- er Gelber’’ Kiepenkerl, Germany). Lupine and maize plants
cation of N in the form of ammonium rather than nitrate will were grown during six weeks in 3.5-L pots and were continu-
increase P uptake when applied together with the struvite. ously monitored in the automatic shoot phenotyping platform
ScreenHouse (Nakhforoosh et al., 2016) at controlled green-
In order to confirm the suggested positive effects of the slow house conditions at the Forschungszentrum in Jülich, IBG-2:
P and N release from struvite on plant performance, an alter- Plant Sciences, Germany (50.89942°N 6.39211°E).
native approach rather than only chemical analyses is now
necessary. Due to major progress in non-invasive shoot phe- Experiment B was conducted subsequently and followed
notyping achieved with imaging sensors (Fiorani and Schurr, Experiment A with minor modifications in which the No P
2013), we could investigate plant leaf area accumulation dur- treatment was replaced with a positive control: fertilization
ing the growth period using an automated shoot-imaging plat- with highly available triple superphosphate (TSP). In Experi-
form and dynamically observe the effect of the slow vs. quick ment B, the number of replicates was reduced to five based
P release at different plant growth stages. on the level of variability we found in Experiment A. Lupine
and maize plants were grown for a period of approximately
We performed a greenhouse study, subdivided into experi- eight weeks.
ment A and B to determine the P fertilizing effect of struvite.
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.com82 Robles-Aguilar, Schrey, Postma, Temperton, Jablonowski J. Plant Nutr. Soil Sci. 2020, 183, 80–90
2.2 Phosphorus sources, fertilization, and 2.3 Plant growing conditions
substrate used Plants were grown under natural light during the day; addi-
The struvite used in this study was provided by Lequia tional assimilation lighting was supplied by mercury lamps
(Girona, Spain). It was recovered from pig manure after (SON–T AGRO 400, Phillips) whenever natural light intensity
anaerobic digestion and solid–liquid separation before was below 400 mmol s–1 m–2, providing a total daily light peri-
biological nitrogen removal. The struvite contained od of 16 h. Average temperature during the experiment was
131.7 mg g–1 P, 5.15 mg g–1 N, and 10.5 mg g–1 Mg; particle 19°C during the day and 17°C at night, with a relative humidity
size: 113 mm. The product used in this study was previously of 60% during the day and 50% at night.
characterized by X-ray diffraction (XRD) analysis as pure
struvite crystals, showing no presence of amorphous sub- All seeds were pre-germinated on filter paper at staggered
stances, contrasted with optic microscope observations, as times between the two species according to their pre-deter-
previously described (Tarragó et al., 2016). For the positive mined germination time. Two seedlings of each species were
control, we used the highly soluble mineral P fertilizer triple transplanted into each pot at a depth of 2 cm. After one week
superphosphate (TSP), containing 45% P2O5, equaling one seedling was removed. The automated watering system
197 g kg–1 P (Van Loon Hoeven, The Netherlands). in both setups (custom-made, Hellmuth Bahrs GmbH & Co.
KG, Brüggen-Bracht, Germany) was adjusted to maintain the
The different P sources were applied to the marginal sandy substrate water content at 50% of its water holding capacity
substrate and were thoroughly mixed in an end-over-end calculated by pot weight every second day. Plants were har-
mixer for 10 min to allow an even distribution of the fertilizers. vested after 40 d of growth in Experiment A and 50 d of
The recycled P as solid struvite powder or highly soluble min- growth in Experiment B. Automated randomization of pot
eral P in the form of solid powder TSP were applied at a rate position was conducted three times per week.
equivalent to 36 mg P per plant (7.2 mg kg –1 substrate) due
to short growth period. The fertilized sand was left undis-
turbed in containers for three days before setting up the 2.4 Data collection on plant performance, nutrient
experiment allowing for equilibration and nutrient distribution. uptake, and pH
Pots with no addition of extra P were set up as the control For each plant, data of plant growth based on projected leaf
(No P). Subsequently, each pot (3.5-L volume) was filled with area were recorded three times per week non-invasively dur-
5 kg of the mixed sand. ing the whole experiment using the automatic shoot pheno-
typing platform ScreenHouse [for detailed description see
Nutrients other than P were supplied through fertigation. As Nakhforoosh et al. (2016)].
the application of struvite accounted for 8 mg of ammonium,
the amount of N applied through fertigation was reduced for At the time of final harvest, i.e., 40 d after sowing in experi-
the struvite treatment, ensuring an equal total N supply in the ment A and 50 d after sowing in experiment B, the heights of
TSP-treatment. Nitrogen was either applied as ammonium the plants were measured. Shoots were separated into
[(NH4)2SO4] or as nitrate [Ca (NO3)2 4H2O and KNO3] to give leaves and stems directly after harvesting, and fresh weights
a final N concentration of 72 mg kg–1 dry substrate. During were determined. Subsequently, the leaf area was measured
the first, third and fifth week of the experiment, plants were using a leaf area meter (Li-3100, Li-cor, Nebraska, USA).
fertigated with nutrient solutions containing all essential Rolled up maize blades were unwound before scanning, but
nutrients but P at increasing concentrations (15, 30, and 55% leaf sheaths were considered as stems.
of modified 1/3 Hoagland solution; Hoagland, 1920), consid-
ering the higher plant N demand due to its increased plant All root samples were carefully washed to remove any
development. The final concentrations (mg kg–1 dry sub- attached substrate. The washed root samples were stored in
strate) were 11.4 Mg, 0.5 Cu, 5 Fe, and 56 K supplied as 50% (v/v) ethanol/water solution until root scanning (Epson
K2SO4 or KNO3. Expression Scan 1680, WinRHIZO STD 1680, Long Beach,
Canada). Data for several root traits, such as total root length,
Plants were grown in nutrient-poor acidic sand (pH 4.8 and root surface area, root diameter, and diameter class length
0.5 mm diameter particle size; Iseke Natursteinbrüche (DCL, root length within a diameter class), were obtained
Bergisch Land GmbH, Wuppertal, Germany). The P concen- using WinRHIZO V.2009 software (Regent Instruments Inc.,
trations in the sand were indicated as suboptimal for plants Quebec, Canada). In experiment A, roots of lupine and maize
(Jordan-Meille et al., 2012) (< 1 mg 100 g–1), analyzed by were analyzed. In experiment B, only lupine roots were ana-
LUFA via CAT method (VDLUFA Method Band I, A 13.1.1, lyzed. The root length was partitioned into 11 diameter
6.4.1). The used sand had a very low organic matter content classes: from < 0.25 to > 3.5 in 0.5-mm increments from root
(< 0.5 g 100 g–1) in order to reduce biological activity that images for each root section. The following parameters were
might interfere with the analyzes of struvite availability in based on observed and/or computed data: root-to-shoot
relation only to the N application or root modifications. In addi- mass ratio (root dry mass / shoot dry mass), specific root
tion, sand drains well and is thereby well suited for fertigation length (SRL) = root length / root dry mass (m g–1), and relative
studies. diameter class length (rDCL) = DCL / root length (yielding a
proportion of root length to normalize disparity between plants
of different sizes).
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.comJ. Plant Nutr. Soil Sci. 2020, 183, 80–90 Effect of N source on P-availability from struvites 83
After the shoot and root measurements, all samples were and N source applied as factors. Tukey’s HSD post-hoc test
dried at 65°C in a forced-draft oven until dry weights were after ANOVAs at p = 0.05 was used to check which level of a
constant and subsequently homogeneously ground. Hundred factor differed from one another. Data were calculated as
mg of the powdered and homogenized plant sample were arithmetic means – standard error of the mean of n = 10 or 5
digested with 3 mL HNO3 and 2 mL H2O2 in the microwave replicates for experiment A and B, respectively.
and made up to a total volume of 14 mL. The samples were
then analyzed for total Mg, P, and K contents by ICP-OES.
The N content was determined by elemental analysis 3 Results
(VarioELcube, Elementar). P uptake efficiency of the various
P sources was calculated with modifications as described by 3.1 Plant growth
Hammond et al. (2009) who defined PUE as the increase
of plant total P content per unit of added P fertilizer Plants subjected to the struvite treatment in Experiment A
(g P plant–1 g–1 P fertilizer). We modified the formula, nor- produced greater shoot biomass than control plants without
malizing the P uptake in the vegetative parts per unit of any P application (Tab. 1). In Experiment B, lupine plants
root length instead of per amount of P applied, renaming the treated with struvite or TSP showed no significant differences
term into ‘‘root P uptake efficiency’’ (PUEr: mg P plant–1 cm in biomass production. In contrast, maize plants subjected to
root). The sand pH was analyzed in a solution of struvite created significantly greater biomass (p < 0.05) than
0.01 M CaCl2 at the end of the experiment. maize treated with TSP (Tab. 1).
We did not observe significantly higher biomass in maize
2.5 Statistical analysis (p = 0.78) or lupine plants grown with ammonium and struvite
compared with nitrate and struvite. In Experiment B, the bio-
Statistical analysis was performed using the statistical pro- mass of lupine plants grown with struvite was even lower with
gram R.2.12.2 (R Core Team, 2012) and biomass yield, leaf ammonium as opposed to nitrate as the N-form. This could
area, nutrient uptake, and root morphological traits were raise concerns about N being limiting, however, the total
measured and were compared with three-way analysis of var- amount of N supplied at the start of the experiment in all treat-
iance (ANOVA), using plant species, P fertilizer treatment,
Table 1: Influence of P fertilizer and N source applied on shoot biomass, shoot P content (P uptake), and shoot P, N, and Mg concentration of
maize and lupine plants growing in acidic sand for Experiment A and B. Values represent the mean of n = 10 for Experiment A, and the mean of
n = 5 for Experiment B. Different letters indicate significant differences at p < 0.05. Mean values with the same letter within the same shoot
parameter and Experiment (A or B) are not significantly different.
Species P source N source Shoot P Shoot P Shoot N Shoot Mg Shoot
content concentration content content biomass
(mg P plant–1) (mg P g plant–1) (mg N plant–1) (mg Mg plant–1) (g)
Experiment A Maize struvite NHþ
4
5.1a 1.5b 83a 15.2a 3.2 – 0.31a
NO
3 4.4a 1.3c 99a 15a 3.2 – 0.42a
No P NHþ
4
0.5d 0.8d 20b 1.4b 0.6 – 0.081c
NO
3 0.4d 0.9c 20b 2.1b 0.5 – 0.11c
Lupine struvite NHþ
4
3.5b 1.9a 68a 7.9ab 1.9 – 0.45b
NO
3 2.5c 1.5bc 63a 8.1ab 1.7 – 0.21b
No P NHþ
4
0.3d 0.9d 16b 1.1b 0.3 – 0.06d
NO
3 0.4d 0.7d 27b 2.1b 0.5 – 0.14c
Experiment B Maize struvite NHþ
4
8.1a 1.1c 98a 32ab 9.7 – 0.84a
NO
3 9.3ab 1.2c 88abc 34a 9.7 – 0.7a
TSP NHþ
4
6.9ab 1.2cc 78bc 27abc 7.8 – 0.82b
NO
3 6.9ab 1.2cc 82abc 31ab 7.9 – 0.74b
Lupine struvite NHþ
4
4.9b 2.3a 61d 12c 2 – 0.3d
NO
3 5.3b 1.9b 93ab 16bc 2.7 – 0.14c
TSP NHþ
4
5.5b 2.1ab 58d 13c 2.5 – 0.63c
NO
3 4.9b 1.8b 73cd 15c 2.4 – 0.28c
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.com84 Robles-Aguilar, Schrey, Postma, Temperton, Jablonowski J. Plant Nutr. Soil Sci. 2020, 183, 80–90
ments was 360 mg N per plant, which is nearly 4 times the lupine plants treated with TSP did not differ from those treated
maximum amount of N taken up, which was 99 mg per plant with struvite (TSP, 263 cm2; struvite, 285 cm2; p < 0.001 as
(Tab. 1). We conclude that N supply was more than sufficient an example for 44 DAS). In maize, a very similar pattern was
to support plant growth and avoid N deficiencies. This conclu- observed. However, the greater leaf area of TSP fertilized
sion is supported by the observation of the plants which did plants during early growth stages was not as strong (1.6%)
not show any signs of chlorosis. Rather, in the No P treat- and occurred later at 24 DAS. From 26 DAS, leaf area
ments nutrient deficiency symptoms were according to typical increased more rapidly in the struvite fertilized plants, which
nutrient deficiency symptoms for P-deficiency: dark green had at the end of the experiment 9.5% more leaf area
and small leaves and slight anthocyanin production in the compared to those fertilized with TSP.
leave sheath of maize (Supplementary material, Figs.
S1–S3). Plant growth also responded strongly to struvite
P-fertilization (Experiment A; Tab. 1). 3.3 Shoot nutrient content
We used shoot P content (mg P plant–1) as an approximate
measure of total P uptake by the plant. Although ammo-
3.2 Non-invasive measurements of leaf area
nium+struvite fertilized plants did not have greater biomass
The total leaf area was estimated from the projected leaf area than nitrate+struvite fertilized plants, we observed greater P
using a calibration curve for which 60 plants were measured uptake by the ammonium+struvite fertilized lupine in Experi-
with the cameras immediately before, and with a leaf area ment A. Even so, the ANOVA results suggest that the N treat-
meter (Li-3100, Li-cor, Nebraska, USA) after harvest. The ment effect on P uptake from struvite is independent of the
obtained calibration curve was linear with a R2 of 0.95. From plant species studied (Tab. 1).
hereon we present total leaf area as estimated based on this
calibration. This response to N form found in Experiment A was not ob-
served in Experiment B. Here, uptake of P from struvite ap-
As observed with the biomass (Tab. 1; Experiment B), struvite plied with nitrate was higher than uptake of P from struvite
treated maize plants had greater leaf area at the end of the when applied with ammonium. In Experiment B we observed
experiment compared to TSP (Fig. 1). For lupine we found no significant differences in P uptake between the plant species.
significant differences in leaf area between struvite- or TSP- The P uptake was higher in maize than in lupine, as maize is
fertilized plants until 44 days after sowing (Fig. 1). Between 9 a faster-growing plant that accumulates more biomass and
to 21 DAS, however, lupine plants had greater leaf area when therefore more total P in the shoots (Tab. 1).
fertilized with TSP compared to struvite. This difference was
greatest at 20 DAS when TSP-fertilized plants had 14% In order to compare both species irrespective of plant size,
greater leaf area. From 21 DAS onwards the leaf area of the shoot P concentration (mg P g plant–1) was analyzed
(A) (B)
Figure 1: Leaf area (cm2) of lupine (A) and maize (B) treated with struvite or TSP, calculated at different
plant stages [Days after sowing (DAS) from 7 to 44]. The differences between ammonium and nitrate treat-
ments are not shown. Struvite treated plants had higher leaf area than TSP at the end of the experiment;
this effect is significant for maize plants (as of 33 DAS). The graph shows the typical growth curve for high-
er plants with an initial slow growth (lag phase), until 25 DAS approximately, then a rapid period of growth
(exponential phase) where maximum growth is seen and the last phase where growth is slow; however,
the plants did not reach a steady phase. Points are averages of n = 5 – standard error of the mean. *signifi-
cant differences between struvite and TSP fertilization.
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.comJ. Plant Nutr. Soil Sci. 2020, 183, 80–90 Effect of N source on P-availability from struvites 85
(Tab. 1). The species had a significant effect on P concentra- lyzes, necessary for calculation of root P uptake efficiency,
tions that were on average greater in lupine than in maize in we focused on lupine plants since we asked if lupine, besides
both experiments. However, P and N fertilization had a much the known physiological root traits that improve the P mobili-
greater effect on shoot P concentrations. In Experiment A, zation making it more suitable for struvite fertilization, might
shoot P concentration was most strongly affected by P ferti- also modify root morphology to further increase struvite-P up-
lization, and within the struvite treatments, ammonium ferti- take. No significant differences were observed for root length
lization resulted in significantly greater P concentrations irrespective of the P form applied.
compared with nitrate. A similar pattern was observed in
Experiment B. However, the N effect on shoot P concentra- The observed increase in root length of nitrate-fertilized plants
tion (TSP or struvite) was only observed in lupine (Tab. 1). was accompanied by greater specific root length (SRL, cm
g–1). Similar to the total root length, this effect was only signifi-
In experiment B, lupine plants treated with struvite+nitrate cant in Experiment A, and an especially large (2-fold)
had a greater N uptake than those treated with ammonium. increase in SRL was observed in struvite-fertilized maize.
No significant differences were observed in the shoot N and
Mg content in any other treatment. Roots of lupine plants showed nodulation in most cases
(approx. 80%) when P was added. The nodulation was higher
in plants treated with nitrate than those treated with ammo-
3.4 Root architecture analyzes nium. However, the differences were not significant.
In Experiment A, both lupine and maize plants fertilized with
struvite had greater root length and root surface area compar-
3.5 P uptake efficiency
ed to those that were unfertilized. We observed an increased
root length and root surface area when plants were fertilized Greater root length may result in greater P uptake. However,
with nitrate, although the magnitude of the effect differed total P uptake is also affected by the root P uptake efficiency
among species and P treatments (Tab. 2). As hypothesized, (PUEr: shoot P content, taken as a proxy of total P uptake,
the largest effect was observed in struvite-fertilized maize, normalized for the total root length, given as mg cm–1). The
which had 78% greater root length when N was applied as root P uptake efficiency was affected by the N and P source
nitrate. applied in our study. In Experiment A, PUEr from struvite was
two (lupine) and three (maize) times higher (p < 0.05) when
In Experiment B, we ask if the observed effect of the applied combined with ammonium than with nitrate (Fig. 2A). We
N source on root morphology (i.e., increased root length and observed a similar trend in Experiment B for struvite (Fig. 2B).
root surface area when plants were fertilized with nitrate) was For TSP there was no effect of N source on PUEr.
also observed with the highly soluble TSP. For the root ana-
Table 2: Root morphological traits (total root length, root surface area, average root diameter, specific root length, and root biomass) of lupine
and maize treated with struvite and affected by the N source applied (NHþ 4 and NO3 ) compared with the No P application (control) in lupine and
maize in Experiment A, and with TSP in lupine in Experiment B. Values are mean (n =10/5) – SEM. Mean values with the same letter within the
same root trait and Experiment (A or B) are not significantly different.
P source N source Total root length Root surface Average root Specific root Root biomass
area diameter length
(cm) (cm2) (mm) (cm mg–1) (g)
Experiment A Lupine Struvite NHþ
4
2167 – 743a 462.7 – 150cd 0.7 – 0.04a 4.6 – 1.03b 0.5 – 0.1a
NO
3 2688 – 512a 611.2 – 139b 0.7 – 0.02a 5.7 – 0.7b 0.4 – 0.1a
No P NHþ
4
553 – 181b 123.5 – 42f 0.7 – 0.05a 5.1 – 0.9b 0.1 – 0.03a
NO
3 995 – 248b 229.8 – 49ef 0.7 – 0.06a 5.0 – 0.9b 0.1 – 0.03a
Maize Struvite NHþ
4
4104– 599d 492.4 – 68bc 0.31 – 0.04b 8.1 – 3.08b 0.5a – 0.06a
NO
3 11430 – 1371c 895.8 – 59a 0.3 – 0.03b 17.5 – 1.75a 0.6a – 0.1a
No P NHþ
4
2949 – 609e 259.9 – 62e 0.3 – 0.07b 14.7 – 4.1a 0.2 – 0.05a
NO
3 3092 – 882de 338.6 – 59de 0.3 – 0.09b 18.2 – 4.6a 0.2 – 0.04a
Experiment B Lupine Struvite NHþ
4
10244.5 – 3535a 5721.4 – 2086a 1.7 – 0.06b 17.2 – 3.1a 0.6 – 0.1a
NO
3 12217.5 – 1220a 7034.3 – 549 a 1.8 – 0.09ab 16.1 – 2.6a 0.8 – 0.08a
TSP NHþ
4
12877.9 – 3326a 7562.1 – 1929a 1.8 – 0.1ab 16.4 – 1.4a 0.7 – 0.1a
NO
3 10295.2 – 3240a 6370 – 1953a 1.9 – 0.03a 13.3 – 2.7a 0.7 – 0.1a
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.com86 Robles-Aguilar, Schrey, Postma, Temperton, Jablonowski J. Plant Nutr. Soil Sci. 2020, 183, 80–90
Figure 2: Root phosphorus uptake efficiency (mg P applied as struvite recovered per cm root) in lupine and maize plants in Experi-
ment A (A), and root phosphorus uptake efficiency (mg P applied as struvite or TSP recovered per cm root) in lupine plants in
Experiment B (B) as affected by the N sources applied (ammonium or nitrate). The positive effect of ammonium applied together
with the struvite in the efficiency of the P uptake, as observed in Experiment A and B in both species is not observed with the TSP
treatment in Experiment B. The line that divides the box represents the median of the data. The end of the box shows the upper
and lower quartiles. The extreme lines out of the box show the highest and lowest value excluding the outliers (shown as dots);
n = 10 for Experiment A and n = 5 for Experiment B. NH4: Ammonium; NO3: Nitrate.
3.6 Substrate pH However, a higher phosphorus uptake efficiency (see discus-
sion below), was not always reflected in higher biomass pro-
The pH of the substrate in Experiment A was significantly
duction in lupine. This result is in accordance with previous
influenced by the N, P, and species treatments. On average,
findings in relation to N uptake (Temperton et al., 2007). Here
the maize substrate had slightly lower pH, nitrate application
a grass species managed to translate higher leaf N when
resulted in higher pH compared to ammonium, and struvite
growing near legumes into higher biomass, whereas a forb
increased pH compared to No P. Lowest pH was observed
did not. This highlights how species-specific the parameter-
in struvite+ammonium fertilized maize and lupine plants
dependent effects can be.
(pH = 4.4), whereas the highest pH was measured in the stru-
vite+nitrate fertilized plants (5.8–6.0 for maize and lupine, re- So far, most of the studies that analyze the slow release
spectively). The modifications of the pH in the sand were not properties of struvite are based on analyzes of the chemical
significant in Experiment B, in which all treatments had pH and physical properties of the product itself, not the effi-
values close to 6.0. We suggest that the longer duration (ten ciency of plant uptake over time (Rahman et al., 2011; Yetil-
more days) of Experiment B might have caused other pro- mezsoy et al., 2013). The new techniques used in our
cesses to have a neutralizing effect on pH. study, in which we monitored the fertilizer effect on leaf
area development during the full experimental growth peri-
od, revealed that initially TSP treatment led to significantly
4 Discussion
higher leaf areas, not observed at the end of the trial. As
demonstrated earlier, different P concentrations supplied to
4.1 Struvite is a sustainable replacement of TSP as the soil significantly influenced leaf area and overall shoot
a slow-release fertilizer biomass (Pang et al., 2010a, 2010b). Therefore, we explain
our observation by the faster initial release of P from TSP
Our results suggest that struvite has the potential to replace
compared with struvite, since all other nutrients were
highly soluble P sources like the commercial TSP. Ours and
equally and sufficiently provided in all setups via nutrient
previous studies confirm that struvite is a good candidate to
solution. For our experimental substrate and plant parame-
be used as a P source for crops or potted plants based on
ters, measurements might indicate that the slower nutrient
biomass production (Johnston and Richards, 2003; Massey
release from struvite (Rahman et al., 2014) could ensure a
et al., 2009; Antonini et al., 2012).
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.comJ. Plant Nutr. Soil Sci. 2020, 183, 80–90 Effect of N source on P-availability from struvites 87
steady nutrient supply according to the needs of the plants, probably invested more in thin roots than those treated with
improving fertilizer efficiency after three weeks. struvite+nitrate, even if it was not translated into a significant
reduction of the average root diameter.
Slow-release of nutrients can contribute to a more sustainable P
fertilization. Environments such as those in, for example, West- A number of previous studies have shown that the availability of
ern Australia, with low P retention in acidic sands (Summers different nutrients can distinctively affect different root morpho-
et al., 1993), fertilizers like struvite with a slow release of P can logical parameters and vice versa. Postma et al. (2014) con-
potentially be used as a nutrient management strategy. cluded that there is a root architectural trade-off for the acquisi-
tion of nitrate and phosphorus, suggesting that roots might modi-
fy the morphology depending on the relative availability of both
4.2 Morphological root adaptations in response to nutrients. In this study the P form did not fundamentally alter the
P and N source responses of root morphology. However, the N form had a large
effect. Furthermore, the level of the effect was plant species-spe-
In our experiments, we provide evidence that struvite treat-
cific. Maize showed greater root morphological plasticity than lu-
ment might limit the P availability during the initial period of
pine. This is in line with our hypothesis relating to lupine possibly
plant growth, triggering a distinct root growth response in
relying more on the release of carboxylates than maize, as previ-
comparison to the quick release P fertilizers like TSP. Unex-
ously described (Robles-Aguilar et al., 2019), with maize relying
pectedly, the P source applied, i.e., struvite or TSP, did not
more on morphological changes.
show a significant effect on the root morphology in Experi-
ment B (Tab. 2).
Besides the P and N effect on root morphology, struvite or
TSP application induce different pH changes in the soil as
Results in the literature about the effect of P on roots show a
well other possible interactions with nutrients, e.g., more Ca
range of different outcomes that are often species-dependent.
provided by TSP versus Mg provided by struvite that explains
For maize, some studies have found that limited P has no sig-
the differences in nutrient availability.
nificant effect on root elongation or lateral root density, but
does have negative effects on emergence of new axial roots
The interactive effects of P and N fertilization in this experi-
(Hajabbasi and Schumacher, 1994; Mollier and Pellerin,
ment might be confounded by the fact that the struvite+nitrate
1999). The decrease in the total root length (TRL) observed
treatments contained a small (8 out of 360 mg per plant)
in Experiment A for maize without added P might be due to a
amount of ammonium from the struvite. We mitigated this
reduction in the emergence of new roots (Tab. 2). In our study,
effect by ensuring that the total amount of N in all treatments
P starvation had no effect on lateral root density in maize,
was the same. However, we could not avoid that the N form in
resulting in the SRL remaining similar to the SRL of struvite-
the nitrate treatments was not 100% pure nitrate. Although
treated plants in Experiment A. Under P starvation, lupine
we regard this effect as small, we cannot fully exclude that
modified its root morphology by increasing primary root elon-
the small amount of ammonium in the struvite+nitrate treat-
gation. A similar observation was made by Wang et al.
ment had no significant effects on growth or root architecture.
(2008), who also described a large number of first-order later-
al roots with probably large amounts of root hairs developed
in lupine grown under low P conditions. This could explain 4.3 Struvite-PUEr is modulated by the nitrogen
why in our study the SRL of lupines without added P
source applied but not the TSP-P
increased in comparison with struvite-treated lupines.
We hypothesized that struvite-P availability would be
The N-source-dependent changes in the root morphology enhanced through rhizosphere acidification, which can be
were similar for both plant species (Tab. 2) and were greater triggered by fertilizing with ammonium (Gahoonia and Niel-
than those resulting from the form of applied P. In Experiment sen, 1992; Marschner, 2011). Consequently, ammonium ferti-
A, struvite-fertilized plants increased the total root length and lization might result in greater P uptake per unit root length
root surface area when they were grown with NO3-N. Nitrate (so called root P uptake efficiency). In the literature there is
application has been reported to increase primary root no consensus on whether the struvite P fertilizer effectiveness
growth, which can be highly correlated in some species with is dependent on the soil or substrate pH. While lower yields
increased total root length (López-Bucio et al., 2003; Gruber have been reported for struvite-treated plants in alkaline sub-
et al., 2013). We expect that this might be the case in lupine, strates [e.g., Brassica napus (Ackerman et al., 2013)], other
as it has a typical legume root system consisting of a domi- studies showed high struvite P fertilizer efficiency in both
nant taproot with a relatively large number of primary lateral acidic and calcareous soils (Möller et al., 2018).
roots and few secondary roots (Clements et al., 1993).
In our study, in agreement with a previous report on maize (Jing
It is known that an increase in root diameter does not corre- et al., 2010), lupine and maize treated with struvite + ammonium
late with an increase in the uptake capacity of NO 3 or NH4
þ
had high P uptake efficiency despite a reduced total root length
(Garnett et al., 2009). In our study, nitrate treated maize (Tab. 2), compared with those treated with struvite + nitrate
increased the SRL in comparison with ammonium in contrast (Fig. 2). We observed a decrease of pH when ammonium was
to lupine. This effect might be explained by an increase in the applied and an increase of pH when nitrate was applied in ex-
number and the average length of lateral roots after nitrate periment A. However, modifications of the pH were not signifi-
application, as previously reported for maize plants (Schorte- cant in Experiment B. As reported earlier (Talboys et al., 2016),
meyer et al., 1993). Lupine treated with struvite+ammonium initial P dissolution rates from struvite decreased significantly
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.com88 Robles-Aguilar, Schrey, Postma, Temperton, Jablonowski J. Plant Nutr. Soil Sci. 2020, 183, 80–90
with increasing pH. However, the slow dissolution of struvite in- observed growth and development during the early vegetative
creased the solution pH itself over time (Talboys et al., 2016). stage (i.e., 5 weeks), whereas effects on yield will have to be
This additional increase of pH might be the reason why struvi- tested in the field on longer time scales. However, our
te+nitrate induced a higher pH change compared with the addi- approach in this experiment was to describe the influence of
tion of ammonium. Furthermore, previous studies have reported the N source applied on the P release from struvite and the
that increased P uptake efficiency by maize with ammonium ap- differences between the two plant species used (lupine and
plication was not only related to a decrease in the soil pH (Hoff- maize) in a marginal acidic substrate. We chose the acidic
mann et al., 1994). This could mean that besides acidification substrate in order to facilitate the struvite-P release, i.e., start-
other mechanisms might play a role, such as stimulating effects ing from a condition that should already be optimal for struvite
of ammonium on the formation of root hairs or other changes in dissolution and resulting potential plant uptake/availability.
root morphology. Overall, this could explain why in experiment B Besides the acidic pH, we chose a marginal mineral sand as
an increase in PUEr was observed when struvite+ammonium the substrate in order to control in which form and amount the
was applied (Fig. 2B), while no pH changes were measured. nutrients were given to the plants.
As was previously discussed, N source applied in our experi- Thomas and Rengel (2002) showed that banding of P and
ment had a greater effect on root morphology than P source. ammonium fertilizers improved P fertilizer use efficiency in P
In agreement with previous studies (e.g., Ma et al., 2013), we fixing soils in comparison with TSP fertilizers. Besides struvite
propose that besides the effect on pH, the enhanced P uptake being an ammonium-phosphorus fertilizer, it still needs to be
by maize, when the P fertilizer was applied together with applied with extra N to totally fulfill a crop’s nutrient demand
ammonium, could be explained by differences in the root spa- due to its low N content. The present study indicates that the
tial distribution. Maize plants, due to a greater root length in use of ammonium-N together with the struvite may facilitate P
the nitrate treatment, had a greater P uptake in comparison acquisition also in acidic P-deficient marginal substrates. This
than those treated with ammonium. However, the higher root was not observed for other highly soluble P sources like TSP,
length of maize in the nitrate treatment resulted in a lower where the plant P use efficiency was not affected by the N
rate of P uptake cm–1 root (PUEr) in comparison with ammo- source applied. The use of highly exudating species might
nium treatment. Therefore, nitrate application might decrease increase the struvite use efficiency, as deduced by the higher
the PUEr in comparison with ammonium. PUEr of lupine compared with maize.
It is known that the root morphological and physiological
responses to P supply or N form applied depend on the plant 5 Conclusions
species (Tranbarger et al., 2003; Hammond et al., 2004; White Different approaches are needed in order to increase the ferti-
et al., 2005). The comparison between species in Experiment A lizer efficiency of struvite or any other recycled P products.
(Fig. 2A) shows that N source applied modified the struvite effect Our study shows that non-invasive phenotyping methods can
in both analyzed species. However, even though in both cases be instrumental for dynamically tracking plant responses to
the ammonium increased the struvite PUEr, lupine showed recycled fertilizers at different plant phenological growth
greater P uptake efficiency compared with maize. A reason why stages. Phenotyping of shoot growth of lupine and maize
lupine showed higher PUEr can be explained by exudation of or- showed that, compared to triple super phosphate (TSP), stru-
ganic acids that occurs in some species (Hinsinger, 2001) such vite-fertilized plants had initially lower leaf area, but plants
as in the lupine used in our study. The exudates, i.e., organic were able to catch up at later stages of the experiment result-
acids among root-induced pH acidification, can displace the ing in similar biomass for lupine or even greater biomass for
phosphate from the soil matrix by ligand exchange increasing maize. To our knowledge, this is the first time a study has
the P availability (Lambers et al., 2006). As shown in a previous been performed in such temporal detail to prove the beneficial
experiment on P recovery from struvite, lupine exudates include slow release properties of struvite on plant performance.
significant amounts of carboxylates, mostly citrate (Robles-
Aguilar et al., 2019). Among the exudation of carboxylates in The hypothesis that the slower rate of P release from struvite
lupine, the biological nitrogen fixation indicated by successful may improve the efficiency of plant P uptake was also sup-
nodulation and its associated soil acidification (Jensen and ported by the higher PUEr from struvite than from TSP. The
Hauggaard-Nielsen, 2003), could be an additional reason for ammonium application compared with the nitrate, increased
the higher PUEr in lupine compared with maize (Fig. 2). These the PUEr of struvite in lupine and maize, an effect not
abilities make lupine a more suitable crop for use of struvite as a observed with the quick available P source TSP. The high
P fertilizer compared to maize. As observed in Experiment B, PUEr with ammonium might be explained by rhizosphere
the use of struvite together with ammonium had a comparable acidification due to ammonium uptake that would favor the
fertilizing effect to TSP in lupine, with efficiency unaffected by the struvite solubilization and the N-dependent modifications in
co-applied N source. the root morphology. A greater root morphological plasticity
was observed in maize than in lupine. It is known that the
Our study provides further support for the need for fertilizer exuded organic acids by some species such as lupine can
management practices in marginal substrates to use appro- displace the phosphate from the matrix by ligand exchange
priate N forms to enhance P-use efficiency. It is likely that increasing the P availability.
changes we observed in the root morphology and PUEr in the
current greenhouse study might deviate from field studies. The use of struvite together with ammonium is recommended to
Especially, the greenhouse studies conducted here only increase the use efficiency of the recycled P. This might not be
ª 2019 The Authors. Journal of Plant Nutrition and Soil Science published by Wiley-VCH Verlag GmbH & Co. KGaA www.plant-soil.comJ. Plant Nutr. Soil Sci. 2020, 183, 80–90 Effect of N source on P-availability from struvites 89
related to an increase in the biomass production in the first stage Gahoonia, T. S., Nielsen, N. E. (1992): The effects of root-induced pH
of the plant growth, but the increase in the P use efficiency might changes on the depletion of inorganic and organic phosphorus in
equal plant yields at a later stage compared to those reached the rhizosphere. Plant Soil 143, 185–191.
with quick-release mineral fertilizers. Thus, we hope that the use Garnett, T., Conn, V., Kaiser, B. N. (2009): Root based approaches to
of struvite as an alternative and sustainable fertilizer will in- improving nitrogen use efficiency in plants. Plant Cell Environ. 32,
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to the recycling of nutrients as well as to a circular bio-economy. Gruber, B. D., Giehl, R. F., Friedel, S., von Wirén, N. (2013): Plasticity
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funded by the European Community’s Framework
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assistance with measurements and trial management and Spracklen, W. P., Greenwood, D. J. (2009): Shoot yield drives
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